Distribution of Antibiotic Resistance Genes in Microbial Communities: the Impact of Anthropogenic Pollution

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Abstract

The review considers issues related to the spread of antibiotic resistance genes in environmental microbial communities. “Hotspots” of adaptive evolution, accumulation and spread of antibiotic-resistant bacteria and genetic material of antibiotic resistance are highlighted. Such “hotspots” include anthropogenic ecosystems, such as municipal wastewater treatment plants, municipal solid waste landfills, livestock enterprises, and agrocenoses. The influence of various types of pollutants and biotic factors on enhancement of mutagenesis and horizontal transfer of antibiotic resistance genes is considered. The role of mobile genetic elements in mobilization and accelerated spread of resistance determinants is shown. Special attention is paid to the role of oxidative stress and stress regulons, which are activated for realization and control of molecular genetic mechanisms of adaptive evolution of bacteria and horizontal distribution of genetic material in bacterial populations. Oxidative stress is identified as one of the main activators of genome destabilization and adaptive evolution of bacteria.

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About the authors

I. S. Sazykin

Southern Federal University

Author for correspondence.
Email: samara@sfedu.ru
Russian Federation, Rostov-on-Don, 344006

M. A. Sazykina

Southern Federal University

Email: samara@sfedu.ru
Russian Federation, Rostov-on-Don, 344006

A. R. Litsevich

Southern Federal University

Email: samara@sfedu.ru
Russian Federation, Rostov-on-Don, 344006

References

  1. Walsh F., Duffy B. (2013) The culturable soil antibiotic resistome: a community of multi-drug resistant bacteria. PloS One. 8(6), e65567. https://doi.org/10.1371/journal.pone.0065567
  2. Pepper I.L. (2013) The soil health-human health nexus. Crit. Rev. Environ. Sci. Technol. 43(24), 2617–2652. https://doi.org/10.1080/10643389.2012.694330
  3. Adu-Oppong B., Gasparrini A. J., Dantas G. (2017) Genomic and functional techniques to mine the microbiome for novel antimicrobials and antimicrobial resistance genes. Ann. N. Y. Acad. Sci. 1388(1), 42–58. https://doi.org/10.1111/nyas.13257
  4. Hu Y., Yang X., Li J., Lv N., Liu F., Wu J., Lin I. Y., Wu N., Weimer B. C., Gao G. F., Liu Y., Zhu B. (2016) The bacterial mobile resistome transfer network connecting the animal and human microbiomes. Appl. Environ. Microbiol. 82(22), 6672–6681. https://doi.org/10.1128/AEM.01802-16
  5. Hsu C., Hsu B., Ji W., Chen J., Hsu T., Ji D., Tseng S., Chiu Y., Kao P., Huang Y. (2015) Antibiotic resistance pattern and gene expression of nontyphoid Salmonella in riversheds. Environ. Sci. Pollut. Res. 22, 7843–7850. https://doi.org/10.1007/s11356-014-4033-y
  6. Pruden A., Pei R., Storteboom H., Carlson K. H. (2006) Antibiotic resistance genes as emerging contaminants: studies in Northern Colorado. Environ. Sci. Technol. 40, 7445–7450. https://doi.org/10.1021/es060413l
  7. Graham D.W., Knapp C.W., Christensen B.T., McCluskey S., Dolfing J. (2016) Appearance of beta-lactam resistance genes in agricultural soils and clinical isolates over the 20th century. Sci. Rep. 6(1), 21550. https://doi.org/10.1038/srep21550
  8. Knapp C.W., Dolfing J., Ehlert P.A., Graham D.W. (2010) Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ. Sci. Technol. 44(2), 580–587. https://doi.org/10.1021/es901221x
  9. Gaze W.H., Krone S.M., Joakim Larrson D.G., Li X.Z., Robinson J.A., Simonet P., Smalla K., Timinouni M., Topp E., Wellington E.M., Wright G.D., Zhu Y.G. (2013) Influence of humans on evaluation and mobilization of environmental antibiotic resistance. Emerging Infect. Dis. 19(7), e120871. https://doi: 10.3201/ eid1907.120871
  10. Zhang R., Yang S., An Y., Wang Y., Lei Y., Song, L. (2022) Antibiotics and antibiotic resistance genes in landfills: a review. Sci. Total Environ. 806(2), 150647. https://doi.org/10.1016/j.scitotenv.2021.150647
  11. Nowrotek M., Jalowiecki L., Harnisz M., Plaza G. A. (2019) Culturomics and metagenomics: in understanding of environmental resistome. Front. Environ. Sci. Eng. 13, 12. https://doi.org/10.1007/s11783-019-1121-8
  12. Li B., Yang Y., Ma L.P., Ju F., Guo F., Tiedje J.M., Zhang T. (2015) Metagenomic and network analysis reveal wide distribution and co-occurrence of environmental antibiotic resistance genes. ISME J. 9, 2490–2502. https://doi.org/10.1038/ismej.2015.59
  13. Yang Y., Li B., Ju F., Zhang T. (2013) Exploring variation of antibiotic resistance genes in activated sludge over a four-year period through a metagenomic approach. Environ. Sci. Technol. 47, 10197–10205. https://doi.org/10.1021/es4017365
  14. Yang Y., Li B., Zou S.C., Fang H.H.P., Zhang T. (2014) Fate of antibiotic resistance genes in sewage treatment plant revealed by metagenomic approach. Water Res. 62, 97–106. https://doi.org/10.1016/j.watres.2014.05.019
  15. Zhao R.X., Feng J., Yin X.L., Liu J., Fu W.J., Berendonk T.U., Zhang T., Li X., Li B. (2018) Antibiotic resistome in landfill leachate from different cities of China deciphered by metagenomic analysis. Water Res. 134, 126–139. https://doi.org/10.1016/j.watres.2018.01.063
  16. Liu X., Yang S., Wang Y.Q., Zhao H.P., Song L.Y. (2018) Metagenomic analysis of antibiotic resistance genes (ARGs) during refuse decomposition. Sci. Total Environ. 634, 1231–1237. https://doi.org/10.1016/j.scitotenv.2018.04.048
  17. Gorecki A., Decewicz P., Dziurzynski M., Janeczko A., Drewniak L., Dziewit L. (2019) Literature-based, manually-curated database of PCR primers for the detection of antibiotic resistance genes in various environments. Water Res. 161, 211–221. https://doi.org/10.1016/j.watres.2019.06.009
  18. Chen Q.L., Li H., Zhou X.Y., Zhao Y., Su J.Q., Zhang X., Huang F.Y. (2017) An underappreciated hotspot of antibiotic resistance: the groundwater near the municipal solid waste landfill. Sci. Total Environ. 609, 966–973. https://doi.org/10.1016/j.scitotenv.2017.07.164
  19. Rizzo L., Manaia C., Merlin C., Schwartz T., Dagot C., Ploy M. C., Michael I., Fatta-Kassinos D. (2013) Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci. Total Environ. 447, 345–360. https://doi.org/10.1016/j.scitotenv.2013.01.032
  20. Ferro G., Guarino F., Castiglione S., Rizzo L. (2016) Antibiotic resistance spread potential in urban wastewater effluents disinfected by UV/H2O2 process. Sci. Total Environ. 560–561, 29–35. https://doi.org/10.1016/j.scitotenv.2016.04.047
  21. Manaia C.M., Rocha J., Scaccia N., Marano R., Radu E., Biancullo F., Cerqueira F., Fortunato G., Iakovides I. C., Zammit I., Kampouris I., Vaz-Moreira I., Nunes O. C. (2018) Antibiotic resistance in wastewater treatment plants: tackling the black box. Environ. Int. 115, 312–324. https://doi.org/10.1016/j.envint.2018.03.044
  22. Manaia C.M., Macedo G., Fatta-Kassinos D., Nunes O.C. (2016) Antibiotic resistance in urban aquatic environments: can it be controlled? Appl. Microbiol. Biotechnol. 100, 1543–1557. https://doi.org/10.1007/s00253-015-7202-0
  23. Di Cesare A., Fontaneto D., Doppelbauer J., Corno G. (2016) Fitness and recovery of bacterial communities and antibiotic resistance genes in urban wastewaters exposed to classical disinfection treatments. Environ. Sci. Technol. 50, 10153–10161. https://doi.org/10.1021/acs.est.6b02268
  24. Kim S., Yun Z., Ha U.H., Lee S., Park H., Kwon E.E., Cho Y., Choung S., Oh J., Medriano C.A., Chandran K. (2014) Transfer of antibiotic resistance plasmids in pure and activated sludge cultures in the presence of environmentally representative micro-contaminant concentrations. Sci. Total Environ. 468–469, 813–820. https://doi.org/10.1016/j.scitotenv.2013.08.100
  25. Carraro E., Bonetta S., Bertino C., Lorenzi E., Bonetta S., Gilli G. (2016) Hospital effluents management: chemical, physical, microbiological risks and legislation in different countries. J. Environ. Manage. 168, 185–199. https://doi.org/10.1016/j.jenvman.2015.11.021
  26. Harris S.J., Cormican M., Cummins C. (2012) Antimicrobial residues and antimicrobial-resistant bacteria: impact on the microbial environment and risk to human health – a review. Hum. Ecol. Risk Assess. 18, 767–809. https://doi.org/10.1080/10807039.2012.688702
  27. Woolhouse M., Ward M., van Bunnik B., Farrar J. (2015) Antimicrobial resistance in humans, livestock and the wider environment. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370, 20140083. https://doi.org/10.1098/rstb.2014.0083
  28. Gu Y., Shen S., Han B., Tian X., Zhang K. (2020) Family livestock waste: an ignored pollutant resource of antibiotic resistance genes. Ecotoxicol. Environ. Saf. 197, 110567. https://doi.org/10.1016/j.ecoenv.2020.110567
  29. Wang Y., Hu Y., Liu F., Cao J., Gao G.F. (2020) Integrated metagenomic and metatranscriptomic profiling reveals differentially expressed resistomes in human, chicken, and pig gut microbiomes. Environ. Int. 138, 105649. https://doi.org/10.1016/j.envint.2020.105649
  30. Brooks J.P., McLaughlin M.R., Gerba C.P., Pepper I.L. (2012) Land application of manure and Class B biosolids: an occupational and public quantitative microbial risk assessment. J Environ. Qual. 41(6), 2009–2023. https://doi.org/10.2134/jeq2011.0430
  31. Lin H., Zhang J., Chen H., Wang J., Sun W., Zhang X., Yang Y., Wang Q., Ma J. (2017) Effect of temperature on sulfonamide antibiotics degradation, and on antibiotic resistance determinants and hosts in animal manures. Sci. Total Environ. 607–608, 725–732. https://doi.org/10.1016/j.scitotenv.2017.07.057
  32. Thanner S., Drissner D., Walsh F. (2016) Antimicrobial resistance in agriculture. mBio. 7, e02227–15. https://doi.org/10.1128/mBio.02227-15
  33. Xie W.Y., Shen Q., Zhao F.J. (2018) Antibiotics and antibiotic resistance from animal manures to soil: a review. Eur. J. Soil Sci. 69, 181–195. https://doi.org/10.1111/ejss.12494
  34. Yazdankhah S., Rudi K., Bernhoft A. (2014) Zinc and copper in animal feed – development of resistance and co-resistance to antimicrobial agents in bacteria of animal origin. Microb. Ecol. Health Dis. 25, 1. https://doi.org/10.3402/mehd.v25.25862
  35. Kivits T., Broers H.P., Beeltje H., van Vliet M., Griffioen J. (2018) Presence and fate of veterinary antibiotics in age-dated groundwater in areas with intensive livestock farming. Environ. Pollut. 241, 988–998. https://doi.org/10.1016/j.envpol.2018.05.085
  36. Manyi-Loh C.E., Mamphweli S.N., Meyer E.L., Makaka G., Simon M., Okoh A.I. (2016) An overview of the control of bacterial pathogens in cattle manure. Int. J. Environ. Res. Public Health. 13(9), 843. https://doi.org/10.3390/ijerph13090843
  37. Xiao R., Huang D., Du L., Song B., Yin L., Chen Y., Gao L., Li R., Huang H., Zeng G. (2023) Antibiotic resistance in soil-plant systems: a review of the source, dissemination, influence factors, and potential exposure risks. Sci. Total Environ. 869, 161855. https://doi.org/10.1016/j.scitotenv.2023.161855
  38. Prestinaci F., Pezzotti P., Pantosti A. (2015) Antimicrobial resistance: a global multifaceted phenomenon. Pathog. Glob. Health. 109, 309–318. https://doi.org/10.1179/2047773215Y.0000000030
  39. Song L.Y., Li L., Yang S., Lan J.W., He H.J., McElmurry S.P., Zhao Y. (2016) Sulfamethoxazole, tetracycline and oxytetracycline and related antibiotic resistance genes in a large-scale landfill, China. Sci. Total Environ. 551, 9–15. https://doi.org/10.1016/j.scitotenv.2016.02.007
  40. Wang Y.Q., Tang W., Qiao J., Song L.Y. (2015) Occurrence and prevalence of antibiotic resistance in landfill leachate. Environ. Sci. Pollut. Res. 22, 12525–12533. https://doi.org/10.1007/s11356-015-4514-7
  41. Wang J.Y., An X.L., Huang F.Y., Su J.Q. (2020) Antibiotic resistome in a landfill leachate treatment plant and effluent-receiving river. Chemosphere. 242, 8. https://doi.org/10.1016/j.chemosphere.2019.125207
  42. Wu D., Ma R.Q., Wei H.W., Yang K., Xie B. (2018) Simulated discharge of treated landfill leachates reveals a fueled development of antibiotic resistance in receiving tidal river. Environ. Int. 114, 143–151. https://doi.org/10.1016/j.envint.2018.02.049
  43. Wu Y., Cui E., Zuo Y., Cheng W., Chen H. (2018) Fate of antibiotic and metal resistance genes during two-phase anaerobic digestion of residue sludge revealed by metagenomic approach. Environ. Sci. Pollut. Res. 25, 13956–13963. https://doi.org/10.1007/s11356-018-1598-x
  44. An X.L., Su J.Q., Li B., Ouyang W.Y., Zhao Y., Chen Q.L., Cui L., Chen H., Gillings M.R., Zhang T., Zhu Y.G. (2018) Tracking antibiotic resistome during wastewater treatment using high throughput quantitative PCR. Environ. Int. 117, 146–153. https://doi.org/10.1016/J.ENVINT.2018.05.011
  45. Wang J., Wang J., Zhao Z., Chen J., Lu H., Liu G., Zhou J., Guan X. (2017) PAHs accelerate the propagation of antibiotic resistance genes in coastal water microbial community. Environ. Pollut. 231, 1145–1152. https://doi.org/10.1016/J.ENVPOL.2017.07.067
  46. Zheng D., Yin G., Liu M., Chen C., Jiang Y., Hou L., Zheng Y. (2021) A systematic review of antibiotics and antibiotic resistance genes in estuarine and coastal environments. Sci. Total Environ. 777, 146009. https://doi.org/10.1016/J.SCITOTENV.2021.146009
  47. Gillings M.R., Gaze W.H., Pruden A., Smalla K., Tiedje J.M., Zhu Y.G. (2015) Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME J. 9(6), 1269–1279. https://doi.org/10.1038/ismej.2014.226
  48. Berendonk T.U., Manaia C.M., Merlin C., Fatta-Kassinos D., Cytryn E., Walsh F., Bürgmann H., Sørum H., Norström M., Pons M.N., Kreuzinger N., Huovinen P., Stefani S., Schwartz T., Kisand V., Baquero F., Martinez J.L. (2015) Tackling antibiotic resistance: the environmental framework. Nat. Rev. Microbiol. 13(5), 310–317. https://doi.org/10.1038/nrmicro3439
  49. Storteboom H., Arabi M., Davis J.G., Crimi B., Pruden A. (2010) Identification of antibiotic-resistance-gene molecular signatures suitable as tracers of pristine river, urban, and agricultural sources. Environ. Sci. Technol. 44(6), 1947–1953. https://doi.org/10.1021/es902893f
  50. Sazykin I.S., Seliverstova E.Yu., Khmelevtsova L.E., Azhogina T.N., Kudeevskaya E.M., Khammami M.I., Gnennaya N.V., Al-Rammahi A.A.K., Rakin A.V., Sazykina M.A. (2019) Occurrence of antibiotic resistance genes in sewages of Rostov-on-Don and lower Don River. Theor. App. Ecol. 4, 76–82. https://doi.org/10.25750/1995-4301-2019-4-076-082
  51. Imlay J.A. (2015) Diagnosing oxidative stress in bacteria: not as easy as you might think. Curr. Opin. Microbiol. 24, 124–31. https://doi.org/10.1016/j.mib.2015.01.004
  52. Li D., Zeng S., He M., Gu A.Z. (2016) Water disinfection byproducts induce antibiotic resistance-role of environmental pollutants in resistance phenomena. Environ. Sci. Technol. 50(6), 3193–3201. https://doi.org/10.1021/acs.est.5b05113
  53. Li M., He Y., Sun J., Li J., Bai J., Zhang C. (2019) Chronic exposure to an environmentally relevant triclosan concentration induces persistent triclosan resistance but reversible antibiotic tolerance in Escherichia coli. Environ. Sci. Technol. 53(6), 3277–3286. https://doi.org/10.1021/acs.est.8b06763
  54. Merchel P., Pereira B., Wang X., Tagkopoulos I. (2021) Biocide-induced emergence of antibiotic resistance in Escherichia coli. Front. Microbiol. 12, 640923. https://doi.org/10.3389/fmicb.2021.640923
  55. Waldron K.J., Robinson N.J. (2009) How do bacterial cells ensure that metalloproteins get the correct metal? Nat. Rev. Microbiol. 7(1), 25–35. https://doi.org/10.1038/nrmicro2057
  56. Gullberg E., Albrecht L.M., Karlsson C., Sandegren L., Andersson D.I. (2014) Selection of a multidrug resistance plasmid by sublethal levels of antibiotics and heavy metals. mBio. 5(5), e01918–14. https://doi.org/10.1128/mBio.01918-14
  57. Seiler C., Berendonk T.U. (2012) Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front. Microbiol. 3, 399. https://doi.org/10.3389/fmicb.2012.00399
  58. Zhu Y.G., Johnson T.A., Su J.Q., Qiao M., Guo G.X., Stedtfeld R.D., Hashsham S.A., Tiedje J.M. (2013) Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc. Natl. Acad. Sci. USA. 110, 3435–3440. https://doi.org/10.1073/pnas.1222743110
  59. Zhao X., Wang J., Zhu L., Wang J. (2019) Field-based evidence for enrichment of antibiotic resistance genes and mobile genetic elements in manure-amended vegetable soils. Sci. Total Environ. 654, 906–913. https://doi.org/10.1016/j.scitotenv.2018.10.446
  60. Lin H., Sun W., Zhang Z., Chapman S.J., Freitag T.E., Fu J., Zhang X., Ma J. (2016) Effects of manure and mineral fertilization strategies on soil antibiotic resistance gene levels and microbial community in a paddy-upland rotation system. Environ. Pollut. 211, 332–337. https://doi.org/10.1016/j.envpol.2016.01.007
  61. Li L.G., Xia Y., Zhang T. (2017) Co-occurrence of antibiotic and metal resistance genes revealed in complete genome collection. ISME J. 11(3), 651–662. https://doi.org/10.1038/ismej.2016.155
  62. Christgen B., Yang Y., Ahammad S.Z., Li B., Rodriquez D.C., Zhang T., Graham D.W. (2015) Metagenomics shows that low-energy anaerobic-aerobic treatment reactors reduce antibiotic resistance gene levels from domestic wastewater. Environ. Sci. Technol. 49(4), 2577–2584. https://doi.org/10.1021/es505521w
  63. Gu M., Imlay J.A. (2011) The SoxRS response of Escherichia coli is directly activated by redox-cycling drugs rather than by superoxide. Mol. Microbiol. 79(5), 1136–1150. https://doi.org/10.1111/j.1365–2958.2010.07520.x
  64. Coba de la Peña T., Redondo F.J., Fillat M.F., Lucas M.M., Pueyo J.J. (2013) Flavodoxin overexpression confers tolerance to oxidative stress in beneficial soil bacteria and improves survival in the presence of the herbicides paraquat and atrazine. J. Appl. Microbiol. 115(1), 236–246. https://doi.org/10.1111/jam.12224
  65. Sazykin I., Naumova E., Azhogina T., Klimova M., Karchava S., Khmelevtsova L., Chernyshenko E., Litsevich A., Khammami M., Sazykina M. (2024) Glyphosate effect on biofilms formation, mutagenesis and stress response of E. сoli. J. Hazard. Mater. 461, 132574. https://doi.org/10.1016/j.jhazmat.2023.132574
  66. Sazykin I.S., Sazykina M.A., Khmelevtsova L.E., Khammami M.I., Karchava Sh.K., Zhuravlev M.V., Kudeevskaya E.M. (2016) Expression of SOD and production of reactive oxygen species in Acinetobacter calcoaceticus caused by hydrocarbons oxidation. Ann. Microbiol. 66(3), 1039–1045. https://doi.org/10.1007/s13213-015-1188-9
  67. Sazykin I.S., Sazykina M.A., Khmelevtsova L.E., Seliverstova E.Yu., Karchava Sh.K., Zhuravleva M.V. (2018) Antioxidant enzymes and reactive oxygen species level of the Achromobacter xylosoxidans bacteria during hydrocarbons biotransformation. Arch. Microbiol. 200(7), 1057–1065. https://doi.org/10.1007/s00203-018-1516-0
  68. Sazykin I., Makarenko M., Khmelevtsova L., Seliverstova E., Rakin A., Sazykina M. (2019) Cyclohexane, naphthalene, and diesel fuel increase oxidative stress, CYP153, sodA, and recA gene expression in Rhodococcus erythropolis. Microbiologyopen. 8(9), e00855. https://doi.org/10.1002/mbo3.855
  69. Kim J., Park W. (2014) Oxidative stress response in Pseudomonas putida. Appl. Microbiol. Biotechnol. 98(16), 6933–6946. https://doi.org/10.1007/s00253-014-5883-4
  70. Pérez-Pantoja D., Nikel P.I., Chavarría M., de Lorenzo V. (2013) Endogenous stress caused by faulty oxidation reactions fosters evolution of 2,4-dinitrotoluene-degrading bacteria. PLoS Genet. 9(8), e1003764. https://doi.org/10.1371/journal.pgen.1003764
  71. Azhogina T., Sazykina M., Konstantinova E., Khmelevtsova L., Minkina T., Antonenko E., Sushkova S., Khammami M., Mandzhieva S., Sazykin I. (2023) Bioaccessible PAH influence on distribution of antibiotic resistance genes and soil toxicity of different types of land use. Environ. Sci. Pollut. Res. 30(5), 12695–12713. https://doi.org/10.1007/s11356-022-23028-2
  72. Ning Q., Wang D., An J., Ding Q., Huang Z., Zou Y., Wu F., You J. (2022) Combined effects of nanosized polystyrene and erythromycin on bacterial growth and resistance mutations in Escherichia coli. J. Hazard. Mater. 422, 126858. https://doi.org/10.1016/j.jhazmat.2021.126858
  73. Høiby N., Bjarnsholt T., Givskov M., Molin S., Ciofu O. (2010) Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents. 35, 322–332. https://doi.org/10.1016/j.ijantimicag.2009.12.011
  74. Jian Z., Zeng L., Xu T., Sun S., Yan S., Yang L., Huang Y., Jia J., Dou T. (2021) Antibiotic resistance genes in bacteria: occurrence, spread, and control. J. Basic Microbiol. 61(12), 1049–1070. https://doi.org/10.1002/jobm.202100201
  75. Partridge S.R., Kwong S.M., Firth N., Jensen S.O. (2018) Mobile genetic elements associated with antimicrobial resistance. Clin. Microbiol. Rev. 31, e00088–17. https://doi.org/10.1128/CMR.00088-17
  76. Vandecraen J., Chandler M., Aertsen A., Houdt R.V. (2017) The impact of insertion sequences on bacterial genome plasticity and adaptability. Crit. Rev. Microbiol. 43, 709–730. https://doi.org/10.1080/1040841X.2017.1303661
  77. Shintani M., Sanchez Z.K., Kimbara K. (2015) Genomics of microbial plasmids: classification and identification based on replication and transfer systems and host taxonomy. Front. Microbiol. 6, 242. https://doi.org/10.3389/fmicb.2015.00242
  78. Mao D., Luo Y., Mathieu J., Wang Q., Feng L., Mu Q., Feng C., Alvarez P.J. (2014) Persistence of extracellular DNA in river sediment facilitates antibiotic resistance gene propagation. Environ. Sci. Technol. 48(1), 71–78. https://doi.org/10.1021/es404280v
  79. Jutkina J., Marathe N.P., Flach C.F., Larsson D.G.J. (2018) Antibiotics and common antibacterial biocides stimulate horizontal transfer of resistance at low concentrations. Sci. Total Environ. 616–617, 172–178. https://doi.org/10.1016/j.scitotenv.2017.10.312
  80. Li Q., Chang W., Zhang H., Hu D., Wang X. (2019) The role of plasmids in the multiple antibiotic resistance transfer in ESBLs-producing Escherichia coli isolated from wastewater treatment plants. Front. Microbiol. 10, 633. https://doi.org/10.3389/fmicb.2019.00633
  81. Che Y., Xia Y., Liu L., Li A.D., Yang Y., Zhang T. (2019) Mobile antibiotic resistome in wastewater treatment plants revealed by Nanopore metagenomic sequencing. Microbiome. 7(1), 44. https://doi.org/10.1186/s40168-019-0663-0
  82. Scanlan P.D. (2017) Bacteria-bacteriophage coevolution in the human gut: implications for microbial diversity and functionality. Trends Microbiol. 25, 614–623. https://doi.org/10.1016/j.tim.2017.02.012
  83. Chen J., Quiles-Puchalt N., Chiang Y.N., Bacigalupe R., Fillol-Salom A., Chee M.S.J., Fitzgerald J.R., Penadés J.R. (2018) Genome hypermobility by lateral transduction. Science. 362, 207–212. https://doi.org/10.1126/science.aat5867
  84. Davies M.R., Holden M.T., Coupland P., Chen J.H., Venturini C., Barnett T.C., Zakour N.L., Tse H., Dougan G., Yuen K.Y., Walker M.J. (2015) Emergence of scarlet fever Streptococcus pyogenes emm12 clones in Hong Kong is associated with toxin acquisition and multidrug resistance. Nat. Genet. 47, 84–87. https://doi.org/10.1038/ng.3147
  85. Haaber J., Penadés J.R., Ingmer H. (2017) Transfer of antibiotic resistance in Staphylococcus aureus. Trends Microbiol. 25, 893‒905. https://doi.org/10.2217/17460913.2.3.323
  86. Shapiro O.H., Kushmaro A., Brenner A. (2010) Bacteriophage predation regulates microbial abundance and diversity in a full-scale bioreactor treating industrial wastewater. ISME J. 4(3), 327–336. https://doi.org/10.1038/ismej.2009.118
  87. Colomer-Lluch M., Calero-Caceres W., Jebri S., Hmaied F., Muniesa M., Jofre J. (2014) Antibiotic resistance genes in bacterial and bacteriophage fractions of Tunisian and Spanish wastewaters as markers to compare the antibiotic resistance patterns in each population. Environ. Int. 73, 167–175. https://doi.org/10.1016/j.envint.2014.07.003
  88. Calero-Caceres W., Muniesa M. (2016) Persistence of naturally occurring antibiotic resistance genes in the bacteria and bacteriophage fractions of wastewater. Water Res. 95, 11–18. https://doi.org/10.1016/j.watres.2016.03.006
  89. Thingstad T.F. (2000) Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol. Oceanogr. 45(6), 1320–1328. https://doi.org/10.4319/lo.2000.45.6.1320
  90. Lang A.S., Westbye A.B., Beatty J.T. (2017) The distribution, evolution, and roles of gene transfer agents in prokaryotic genetic exchange. Annu. Rev. Virol. 4, 87–104. https://doi.org/10.1146/annurev-virology-101416-041624
  91. Solioz M., Marrs B. (1977) The gene transfer agent of Rhodopseudomonas capsulata. Purification and characterization of its nucleic acid. Arch. Biochem. Biophys. 181, 300–307. https://doi.org/10.1016/0003-9861(77)90508-2
  92. Brown-Jaque M., Calero-Cáceres W., Muniesa M. (2015) Transfer of antibiotic-resistance genes via phage-related mobile elements. Plasmid. 79, 1–7. https://doi.org/10.1016/j.plasmid.2015.01.001
  93. Lang A.S., Zhaxybayeva O., Beatty J.T. (2012) Gene transfer agents: phage-like elements of genetic exchange. Nat. Rev. Microbiol. 10, 472–482. https://doi.org/10.1038/nrmicro2802
  94. Guy L., Nystedt B., Toft C., Zaremba-Niedzwiedzka K., Berglund E.C., Granberg F., Näslund K., Eriksson A.S., Andersson S.G. (2013) A gene transfer agent and a dynamic repertoire of secretion systems hold the keys to the explosive radiation of the emerging pathogen Bartonella. PLoS Genet. 9, e1003393. https://doi.org/10.1371/journal.pgen.1003393
  95. McDaniel L.D, Young E., Delaney J., Ruhnau F., Ritchie K.B., Paul J.H. (2010) High frequency of horizontal gene transfer in the oceans. Science. 330, 50. https://doi.org/10.1126/science.1192243
  96. Marrs B. (1974) Genetic recombination in Rhodopseudomonas capsulata. Proc. Natl. Acad. Sci. USA. 71, 971–973. https://doi.org/ 10.1073/pnas.71.3.971
  97. Bárdy P., Füzik T., Hrebík D., Plevka P. (2020) Structure and mechanism of DNA delivery of a gene transfer agent. Nat. Commun. 11, 3034. https://doi.org/10.1038/s41467-020-16669-9
  98. Mirajkar N.S., Gebhart C.J. (2014) Understanding the molecular epidemiology and global relationships of Brachyspira hyodysenteriae from swine herds in the United States: a multi-locus sequence typing approach. PLoS One. 9, e107176. https://doi.org/10.1371/journal.pone.0107176
  99. Christensen S., Serbus L.R. (2020) Gene transfer agents in symbiotic microbes. Results Probl. Cell Differ. 69, 25–76. https://doi.org/10.1007/978-3-030-51849-3_2
  100. Baharoglu Z., Mazel D. (2014) SOS, the formidable strategy of bacteria against aggressions. FEMS Microbiol. Rev. 38(6), 1126–1145. https://doi.org/10.1111/1574-6976.12077
  101. Napolitano R., Janel-Bintz R., Wagner J., Fuchs R.P. (2000) All three SOS-inducible DNA polymerases (Pol II, Pol IV and Pol V) are involved in induced mutagenesis. EMBO J. 19(22), 6259–6265. https://doi.org/10.1093/emboj/19.22.6259
  102. Pagès V., Fuchs R.P. (2003) Uncoupling of leading- and lagging-strand DNA replication during lesion bypass in vivo. Science. 300(5623), 1300–1303. https://doi.org/10.1126/science.1083964
  103. Baharoglu Z., Mazel D. (2011) Vibrio cholerae triggers SOS and mutagenesis in response to a wide range of antibiotics: a route towards multiresistance. Antimicrob. Agents Chemother. 55(5), 2438–2441. https://doi.org/10.1128/AAC.01549-10
  104. Boles B.R., Singh P.K. (2008) Endogenous oxidative stress produces diversity and adaptability in biofilm communities. Proc. Natl. Acad. Sci. USA. 105(34), 12503–12508. https://doi.org/10.1073/pnas.0801499105
  105. Chen X., Yin H., Li G., Wang W., Wong P.K., Zhao H., An T. (2019) Antibiotic-resistance gene transfer in antibiotic-resistance bacteria under different light irradiation: implications from oxidative stress and gene expression. Water Res. 149, 282–291. https://doi.org/10.1016/j.watres.2018.11.019
  106. Hocquet D., Llanes C., Thouverez M., Kulasekara H.D., Bertrand X., Plésiat P., Mazel D., Miller S.I. (2012) Evidence for induction of integron-based antibiotic resistance by the SOS response in a clinical setting. PLoS Pathog. 8 (6), e1002778. https://doi.org/10.1371/journal.ppat.1002778
  107. Soucy S.M., Huang J., Gogarten J.P. (2015) Horizontal gene transfer: building the web of life. Nat. Rev. Genet. 16, 472–482. https://doi.org/10.1038/nrg3962
  108. Schönknecht G., Chen W.H., Ternes C.M., Barbier G.G., Shrestha R.P., Stanke, M., Bräutigam A., Baker B.J., Banfield J.F., Garavito R.M., Carr K., Wilkerson C., Rensing S.A., Gagneul D., Dickenson N.E., Oesterhelt C., Lercher M.J., Weber A.P. (2013) Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science. 339, 1207–1210. https://doi.org/10.1126/science.1231707
  109. Lin M., Kussell E. (2019) Inferring bacterial recombination rates from large-scale sequencing datasets. Nat. Methods. 16, 199–204. https://doi.org/10.1038/s41592-018-0293-7
  110. Niehus R., Mitri S., Fletcher A.G., Foster K.R. (2015) Migration and horizontal gene transfer divide microbial genomes into multiple niches. Nat. Commun. 6, 8924. https://doi.org/10.1038/ncomms9924
  111. Power J.J., Pinheiro F., Pompei S., Kovacova V., Yüksel M., Rathmann I., Förster M., Lässig M., Maier B. (2021) Adaptive evolution of hybrid bacteria by horizontal gene transfer. Proc. Natl. Acad. Sci. USA. 118, e2007873118. https://doi.org/ 10.1073/pnas.2007873118
  112. Chiang S.M., Schellhorn H.E. (2012) Regulators of oxidative stress response genes in Escherichia coli and their functional conservation in bacteria. Arch. Biochem. Biophys. 525(2), 161–169. https://doi.org/10.1016/j.abb.2012.02.007
  113. Moore J.M., Correa R., Rosenberg S.M., Hastings P.J. (2017) Persistent damaged bases in DNA allow mutagenic break repair in Escherichia coli. PLoS Genet. 13(7), e1006733. https://doi.org/10.1371/journal.pgen.1006733
  114. Pribis J.P., García-Villada L., Zhai Y., Lewin-Epstein O., Wang A.Z., Liu J., Xia J., Mei Q., Fitzgerald D.M., Bos J., Austin R.H., Herman C., Bates D., Hadany L., Hastings P.J., Rosenberg S. M. (2019) Gamblers: an antibiotic-induced evolvable cell subpopulation differentiated by reactive-oxygen-induced general stress response. Mol. Cell. 74(4), 785–800.e7. https://doi.org/10.1016/j.molcel.2019.02.037
  115. Bos J., Zhang Q., Vyawahare S., Rogers E.., Rosenberg S.M., Austin R.H. (2015) Emergence of antibiotic resistance from multinucleated bacterial filaments. Proc. Natl. Acad. Sci. USA. 112(1), 178–183. https://doi.org/10.1073/pnas.1420702111
  116. Glaeser J., Zobawa M., Lottspeich F., Klug G. (2007) Protein synthesis patterns reveal a complex regulatory response to singlet oxygen in Rhodobacter. J. Proteome Res. 6, 2460–2471. https://doi.org/10.1021/pr060624p
  117. Campbell E.A., Greenwell R., Anthony J.R., Wang S., Lim L., Das K., Sofia H.J., Donohue T.J., Darst S.A. (2007) A conserved structural module regulates transcriptional responses to diverse stress signals in bacteria. Mol. Cell. 27, 793–805. https://doi.org/10.1016/j.molcel.2007.07.009
  118. Nuss A.M., Glaeser J., Klug G. (2009) RpoHII activates oxidative-stress defense systems and is controlled by RpoE in the singlet oxygen-dependent response in Rhodobacter sphaeroides. J. Bacteriol. 191, 220–230. https://doi.org/10.1128/JB.00925-08
  119. Nuss A.M., Glaeser J., Berghoff B.A., Klug G. (2010) Overlapping alternative sigma factor regulons in the response to singlet oxygen in Rhodobacter sphaeroides. J. Bacteriol. 192, 2613–2623. https://doi.org/10.1128/JB.01605-09
  120. Adnan F., Weber L., Klug G. (2015) The sRNA SorY confers resistance during photooxidative stress by affecting a metabolite transporter in Rhodobacter sphaeroides. RNA Biol. 12, 569–577. https://doi.org/10.1080/15476286.2015.1031948
  121. Peng T., Berghoff B.A., Oh J.I., Weber L., Schirmer J., Schwarz J., Glaeser J., Klug G. (2016) Regulation of a polyamine transporter by the conserved 3′ UTR-derived sRNA SorX confers resistance to singlet oxygen and organic hydroperoxides in Rhodobacter sphaeroides. RNA Biol. 13, 988–999. https://doi.org/10.1080/15476286.2016.1212152
  122. Jitprasutwit S., Ong C., Juntawieng N., Ooi W.F., Hemsley C.M., Vattanaviboon P., Titball R.W., Tan P., Korbsrisate S. (2014) Transcriptional profiles of Burkholderia pseudomallei reveal the direct and indirect roles of Sigma E under oxidative stress conditions. BMC Genomics. 15(1), 787. https://doi.org/10.1186/1471-2164-15-787
  123. Ahmed M.N., Porse A., Abdelsamad A., Sommer M., Høiby N., Ciofu O. (2019) lack of the major multifunctional catalase KatA in Pseudomonas aeruginosa accelerates evolution of antibiotic resistance in ciprofloxacin-treated biofilms. Antimicrob. Agents Chemother. 63(10), e00766–19. https://doi.org/10.1128/AAC.00766-19
  124. Tavita K., Mikkel K., Tark-Dame M., Jerabek H., Teras R., Sidorenko J., Tegova R., Tover A., Dame R.T., Kivisaar M. (2012) Homologous recombination is facilitated in starving populations of Pseudomonas putida by phenol stress and affected by chromosomal location of the recombination target. Mutat. Res. 737(1–2), 12–24. https://doi.org/10.1016/j.mrfmmm.2012.07.004
  125. Akkaya Ö., Pérez-Pantoja D.R., Calles B., Nikel P.I., de Lorenzo V. (2018) The metabolic redox regime of Pseudomonas putida tunes its evolvability toward novel xenobiotic substrates. MBio. 9(4), e01512–18. https://doi.org/10.1128/mBio.01512-18
  126. Akkaya Ö., Nikel P.I., Pérez-Pantoja D., de Lorenzo V. (2019) Evolving metabolism of 2,4-dinitrotoluene triggers SOS-independent diversification of host cells. Environ. Microbiol. 21(1), 314–326. https://doi.org/10.1111/1462-2920.14459

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